The γ-Carbonic Anhydrase Subcomplex of Mitochondrial Complex I Is Essential for Development and Important for Photomorphogenesis of Arabidopsis

Complex I (NADH:ubiquinone oxidoreductase) is the entry point for electrons into the respiratory electron transport chain; therefore, it plays a central role in cellular energy metabolism. Complex I from different organisms has a similar basic structure. However, an extra structural module, referred to as the gamma-carbonic anhydrase (gamma CA) subcomplex, is found in the mitochondrial complex I of photoautotrophic eukaryotes, such as green alga and plants, but not in that of the heterotrophic eukaryotes, such as fungi and mammals. It has been proposed that the gamma CA subcomplex is required for the light-dependent life style of photoautotrophic eukaryotes, but this hypothesis has not been successfully tested. We report here a genetic study of the genes gamma CAL1 and gamma CAL2 that encode two subunits of the gamma CA subcomplex of mitochondrial complex I. We found that mutations of gamma CAL1 and gamma CAL2 in Arabidopsis (Arabidopsis thaliana) result in defective embryogenesis and nongerminating seeds, demonstrating the functional significance of the gamma CA subcomplex of mitochondrial complex I in plant development. Surprisingly, we also found that reduced expression of gamma CAL1 and gamma CAL2 genes altered photomorphogenic development. The gamma cal1 mutant plant expressing the RNA interference construct of the gamma CAL2 gene showed a partial constitutive photomorphogenic phenotype in young seedlings and a reduced photoperiodic sensitivity in adult plants. The involvement of the gamma CA subcomplex of mitochondrial complex I in plant photomorphogenesis and the possible evolutionary significance of this plant-specific mitochondrial protein complex are discussed.